Nutritional Bioavailability of Manganese - ACS Publications

Chapter 1

Manganese Bioavailability Overview Constance Kies

Downloaded by UNIV OF SYDNEY on August 21, 2013 | http://pubs.acs.org Publication Date: October 5, 1987 | doi: 10.1021/bk-1987-0354.ch001

Department of Human Nutrition and Food Service Management, University of Nebraska, Lincoln, NE 68583

Manganese is recognized as an essential nutrient for humans and animals; however, in excessive amounts manganese is also a toxic substance. Manganese has been defined as being a component of several enzymes and an activator of several other enzyme systems although other minerals such as magnesium can substitute for manganese in many but not all of these metabolic processes. Since nutritional adequacy of manganese is necessary for the enzyme manganese superoxide dismutase, research dealing with this enzyme is of current interest. Only one case of frank manganese deficiency in the human has been identified and publicized in the literature. However, animal studies indicate that manganese deficiencies affect bone, brain and reproductive systems. Manganese absorption from the gastrointestinal tract is thought to be poor but its absorption is thought to be at least in part governed by its valence state. In the United States recent research suggests that mean manganese intakes of women are considerably lower than are the NRC Estimated Safe and Adequate Daily Dietary Intakes while those of formula fed infants are greater than the NRC ESADDI listings for this age group. Depending upon manganese source and availability of manganese from these sources, manganese adequacy or toxicity might be a problem for these segments of the American population. Manganese has been found t o be an e s s e n t i a l n u t r i e n t f o r t h e human as w e l l as f o r many o t h e r l i v i n g o r g a n i s m s ; however, i n e x c e s s i v e amounts, i t i s a l s o a t o x i c m a t e r i a l ( 1 - 6 ) . D e f i c i e n c y symptoms f o r manganese i n s e v e r a l s p e c i e s have been c r e a t e d and manganese m e t a b o l i c r o l e s have, a t l e a s t i n p a r t , been d e f i n e d (5,7-15). So c a l l e d "normal" manganese c o n c e n t r a t i o n s i n b l o o d have been e s t a b l i s h e d (1,10,16). K i n e t i c s o f manganese uptake and m e t a b o l i s m by

0097-6156/87/0354-0001 $06.00/0 © 1987 American Chemical Society

In Nutritional Bioavailability of Manganese; Kies, C.; ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

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NUTRITIONAL BIOAVAILABILITY OF MANGANESE

t i s s u e s under c o n d i t i o n s o f manganese t o x i c i t y and d e f i c i e n c y have been reviewed by Keen and L o n n e r d a l i n t h i s volume.


Manganese Enzymes Systems Manganese i s a component o f p y r u v a t e c a r b o x y l a s e and m i t o c h o n d r i a l s u p e r o x i d e dismutase and a c t i v a t e s a number o f enzymes i n c l u d i n g p h o s p h a t a s e s , k i n a s e s , d e c a r b o x y l a s e s , and g l y c o s y l t r a n s f e r a s e s t h a t are i n v o l v e d i n t h e s y n t h e s i s o f p o l y s a c c h a r i d e s and g l y c o p r o t e i n s (12,17,18). I t i s a s s o c i a t e d w i t h the s y n t h e s i s o f p r o t e i n , DNA, and RNA w i t h c a r t i l e g e m u c o p o l y s a c c h a r i d e s y n t h e s i s (5,19). Since i s has a l s o been shown t o be i n v o l v e d i n amino a c i d t r a n s p o r t and c a t a b o l i s m , t h i s s u g g e s t s t h a t i n c r e a s e d p r o t e i n i n t a k e might i n c r e a s e t h e need f o r manganese i n t h e t i s s u e s ( 5 ) . R e c e n t l y , i n v e s t i g a t i o n s o f f a c t o r s a f f e c t i n g a c t i v i t y l e v e l s and f u n c t i o n s o f manganese s u p e r o x i d e dismutase have been p a r t i c u l a r l y a c t i v e . S u p e r o x i d e d i s m u t a s e s , enzymes f u n c t i o n i n g t o p r o t e c t c e l l membranes from l i p i d p e r o x i d a t i o n , have been found t o e x i s t i n two forms, one c o n t a i n i n g manganese and t h e o t h e r c o n t a i n i n g copper and z i n c ( 2 0 ) . A r e l a t i o n s h i p between manganese consumption and supero x i d e dismutase a c t i v i t y has been found. H e p a t i c c o n c e n t r a t i o n s o f manganese and h e p a t i c manganese s u p e r o x i d e dismutase a c t i v i t i e s were h i g h e r but h e p a t i c c o p p e r - z i n c d i s m u t a s e l e v e l s were lower i n e t h a n o l fed monkeys than i n c o n t r o l monkeys ( 2 1 ) . When d i f f e r e n t groups o f w e a n l i n g r a t s were f e d r a t i o n s cont a i n i n g graded l e v e l s o f manganese r a n g i n g from 0.2 t o 29.7 mg/kg o f r a t i o n , s i g n i f i c a n t c o r r e l a t i o n s between d i e t a r y manganese l e v e l s w i t h h e a r t and k i d n e y manganese s u p e r o x i d e dismutase enzyme a c t i v i t i e s , l i v e r a r g i n a s e and plasma a l k a l i n e phosphatase a c t i v i t i e s and h e a r t , k i d n e y , l i v e r and plasma manganese c o n c e n t r a t i o n s were found; however, no changes o c c u r r e d i n t h e a c t i v i t i e s o f c o p p e r - c o n t a i n i n g superoxide dismutase o r g l u t a t h i o n e peroxidase i n the t i s s u e analyzed (22). I n manganese d e f i c i e n c y i n t h e c h i c k e n , manganese i s r e p l a c e d w i t h magnesium so t h a t no l o s s o f p y r u v a t e c a r b o x y l a s e o c c u r s ( 2 3 ) . DeRosa e t a l . (18) v e r i f i e d a d e c r e a s e i n manganese s u p e r o x i d e d i s mutase a c t i v i t y i n manganese d e f i c i e n t r a t s and mice. ZidenbergCherr e t a l . (17) r e p o r t e d t h a t l i p i d p e r o x i d a t i o n i n c r e a s e d t o a g r e a t e r e x t e n t i n m a n g a n e s e - d e f i c i e n t than i n m a n g a n e s e - s u f f i c i e n t r a t s . C o n c u r r e n t l y manganese s u p e r o x i d e dismutase a c t i v i t y i n c r e a s e d to a much l e s s e r e x t e n t i n t h e d e f i c i e n t animals (17) • Hence, m i t o c h o n d r i a l membrane damage found i n manganese d e f i c i e n t a n i m a l s might be due t o i n c r e a s e d f r e e r a d i c a l p r o d u c t i o n due t o depressed manganese s u p e r o x i d e dismutase a c t i v i t y . Manganese D e f i c i e n c y Symptoms Manganese d e f i c i e n c y symptoms i n animals a f f e c t t h r e e systems - bone, r e p r o d u c t i v e and b r a i n (6,24). Impaired growth, s k e l e t a l abnormali t i e s , depressed r e p r o d u c t i v e f u n c t i o n and a t a x i a i n newborn appear to be s i m i l a r manganese symptoms i n a l l s p e c i e s s t u d i e d . The s i n g l e r e p o r t e d case o f f r a n k manganese d e f i c i e n c y i n humans a r o s e u n i n t e n t i o n a l l y i n an a d u l t male p a r t i c i p a t i n g i n a v i t a m i n K d e f i c i e n c y study ( 2 5 ) . I n a d v e r t e n t l y manganese was o m i t t e d from t h e p u r i f i e d diet mixture. The s i g n s and symptoms o f w e i g h t l o s s ,


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KIES

Manganese Bioavailability Overview

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t r a n s i e n t d e r m a t i t i s , nausea, slow growth and r e d d e n i n g o f the h a i r and b e a r d , h y p o c h o l e s t e r o l e m i a and depressed v i t a m i n K depending c l o t t i n g f a c t o r s d i d not respond t o v i t a m i n K t h e r a p y but were c o r r e c t e d by the a d m i n i s t r a t i o n of manganese. Because o f the b l o o d l o w e r i n g c h o l e s t e r o l e f f e c t s o f a manganese d e f i c i e n c y , involvement o f manganese i n l i p i d m e t a b o l i s m has been a t o p i c o f r e s e a r c h i n t e r e s t a s reviewed by Johnson and K i e s i n t h i s volume.


Manganese A b s o r p t i o n and E x c r e t i o n Manganese i s o n l y p o o r l y absorbed from the i n t e s t i n a l t r a c t ; howe v e r , a b s o r p t i o n o c c u r s i n t o mucosa c e l l s throughout the s m a l l i n t e s t i n e s (13,26). E x c r e t i o n of manganese through b i l e and panc r e a t i c j u i c e i s a p p a r e n t l y more i m p o r t a n t than a b s o r p t i o n i n maintenance of manganese h o m e o s t a s i s a l t h o u g h young a n i m a l s seem t o l a c k the a b i l i t y t o e x c r e t e manganese. Manganese i s a p p a r e n t l y absorbed i n the +2 v a l e n c e s t a t e and competes w i t h i r o n and c o b a l t f o r the same a b s o r p t i o n s i t e s (27) . Mechanisms of manganese uptake and r e t e n t i o n both i n e x p e r i m e n t a l a n i m a l s and humans a r e d i s c u s s e d i n the c h a p t e r by Keen et a l . Three o f the many d e t e r m i n a n t s o f manganese a b s o r p t i o n and r e t e n t i o n a r e : 1) d e v e l o p m e n t a l s t a t u s ; 2) d i e t a r y c o n s t i t u e n t s ; and 3) membrane t r a n s l o c a t i o n of the element. However, much o f the i n f o r m a t i o n on manganese a b s o r p t i o n has been o b t a i n e d from a n i m a l s t u d i e s w i t h the a s s u m p t i o n made t h a t t h e s e mechanisms a l s o a p p l y t o humans. Other n u t r i e n t s have been found t o i n f l u e n c e the a b s o r p t i o n o f manganese. Manganese a b s o r p t i o n has been found t o be a s s o c i a t e d w i t h h i g h i n t a k e s o f d i e t a r y c a l c i u m a s d i s c u s s e d by McDermott and K i e s i n t h i s volume. The p o s s i b l e r e l a t i o n s h i p s o f c a l c i u m , manganese and bone h e a l t h may be o f importance i n the o c c u r r e n c e o f o s t e o p o r o s i s as d i s c u s s e d by S t r a u s s and Saltman i n another c h a p t e r . S i n c e i r o n and manganese compete f o r b i n d i n g s i t e s i n the i n t e s t i n e s i t i s not s u r p r i s i n g t h a t d i e t a r y i r o n a p p a r e n t l y i n h i b i t s manganese u t i l i z e d a s d i s c u s s e d i n the c h a p t e r by Gruden. D i e t a r y Manganese Needs and I n t a k e s o f Humans Because o f a l a c k of i n f o r m a t i o n on manganese c o n t e n t s o f f o o d s , manganese i n t a k e s a r e not u s u a l l y i n c l u d e d i n n u t r i e n t i n t a k e s u r v e y s . However, the s e v e r a l s u r v e y s w h i c h have been done i n the U n i t e d S t a t e s and i n the U n i t e d Kingdom have y i e l d e d somewhat s i m i l a r r e s u l t s r e g a r d i n g u s u a l manganese i n t a k e s of human a d u l t p o p u l a t i o n s . Schroeder et a l . (6) e s t i m a t e d manganese i n t a k e s t o be between 2.2 and 8.8 mg/day; Wenlock e t a l . (28) e s t i m a t e d mean i n t a k e s t o be 4.6 mg/day and W a s l i e n (29) found i n t a k e s t o range from 0.9 t o 7.0 mg/ day. U s i n g a n a l y z e d , model U.S. d i e t s , P e n n i n g t o n et a l . (30) found a d u l t i n t a k e s o f manganese t o range from 3.52 t o 3.67 mg/day d u r i n g the 1977-1982 time p e r i o d . A t the U n i v e r s i t y of N e b r a s k a , manganese i n t a k e s o f young c o l l e g e women consuming s e l f - s e l e c t e d d i e t s ranged from 0.8 t o 5.2 mg/day w i t h a mean o f 1.28 mg/day a s e s t i m a t e d from one week d i e t a r y d i a r i e s and from a n a l y s e s o f manganese c o n t e n t s o f feces (31). An i n t e r e s t i n g r e c e n t paper (32) i n c l u d e d not o n l y a n a l y z e d manganese c o n t e n t s o f a l a r g e number o f foods based on an e x c e l l e n t


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s a m p l i n g p r o c e d u r e b u t a l s o i n c l u d e d e s t i m a t e d mean manganese l e v e l s of e i g h t age-sex group d i e t s compared w i t h t h e NRC E s t i m a t e d Safe and Adequate D a i l y D i e t a r y I n t a k e s (ESADDI). The mean i n t a k e o f 1.10 mg manganese/day f o r 6-11 month i n f a n t s s l i g h t l y exceeded t h e ESADDI and t h a t f o r t h e two-year o l d c h i l d was on t h e v e r y h i g h end o f t h e s c a l e (a mean i n t a k e o f 1.47 r e l a t e d t o a ESADDI s c a l e o f 1.001.50). F o r a l l o f t h e male g r o u p , t h e mean manganese i n t a k e s were w i t h i n t h e range l i m i t s o f t h e ESADDI s b u t were toward t h e lower end of t h e s c a l e . F o r a l l female g r o u p s , t h e mean manganese i n t a k e s were c o n s i d e r a b l y below t h e ESADDI s• S i n c e t h e ESADDI s f o r men and women a r e t h e same, t h e low i n t a k e s o f manganese o f women i n compari s o n t o t h e ESADDI s a r e i n p a r t due t o t h e lower food i n t a k e s o f women due t o l o w e r c a l o r i c needs. However, t h e s e d a t a do suggest t h a t manganese i n t a k e s f o r many Americans may be s e r i o u s l y l o w . f

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T


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Manganese Content o f M i l k and I n f a n t Formulas E s t i m a t i o n o f manganese i n t a k e s o f i n f a n t s has been an a r e a o f p a r t i c u l a r r e s e a r c h i n t e n s i t y . W h i l e e s t i m a t i o n s o f manganese content o f human m i l k v a r y , t h e r e i s g e n e r a l agreement t h a t t h e manganese content o f human m i l k i s s u b s t a n t i a l l y lower than t h a t o f cow's m i l k ( 3 3 ) . Manganese i n cow's m i l k i s combined w i t h d i f f e r e n t and s m a l l e r p r o t e i n m o l e c u l e s t h a n i s t h a t o f human m i l k (34-36). Degree o f a b s o r p t i o n may be d i f f e r e n t depending upon l i g a n b i n d i n g i n t h i s m i l k and may be d i f f e r e n t than t h a t o f f r e e manganese from s u p p l e m e n t a l manganese s a l t s . T h i s has c r e a t e d something o f a dilemma f o r p r o d u c e r s o f i n f a n t f o r m u l a s f o r b o t t l e f e e d i n g w h i c h has l e d t o a d i v e r s i t y o f l e v e l s o f manganese content i n t h e s e p r o d u c t s . S i n c e human m i l k , cow's m i l k and/or f o r m u l a a r e t h e p r i n c i p a l foods consumed by i n f a n t s , manganese i n t a k e s a r e determined t o a l a r g e e x t e n t by t h e q u a n t i t a t i v e manganese c o n t e n t s o f t h e s e s u b s t a n c e s . B r e a s t m i l k - f e d i n f a n t s , t h e r e f o r e , have l o w e r i n t a k e s o f manganese t h a n those f e d cow's m i l k f o r m u l a s b u t whether o r n o t t h e manganese i s e q u a l l y a v a i l a b l e i s unknown. I n t h i s book, L o n n e r d a l e t a l . p r e s e n t e v i dence t h a t manganese r e t e n t i o n from m i l k and from m i l k f o r m u l a s i s h i g h w h i l e t h a t from soy f o r m u l a s i s much l o w e r . Manganese C o n t e n t s o f Foods Foods v a r y i n t h e i r c o n t e n t s o f manganese (32,37,38). Comparisons o f manganese c o n t e n t s o f d i f f e r e n t foods a r e g i v e n i n T a b l e I . P l a n t o r i g i n foods such as t e a , whole g r a i n c e r e a l s , some dark green l e a f y v e g e t a b l e s , and n u t s c o n t a i n h i g h amounts o f manganese. Howe v e r , t h e s e p r o d u c t s o f t e n c o n c u r r e n t l y c o n t a i n h i g h amounts o f t a n n i n s , o x a l a t e s , p h y t a t e s and f i b e r . These d i e t a r y c o n s t i t u e n t s have been found t o i n h i b i t t h e a b s o r p t i o n o f o t h e r m i n e r a l s ; hence, might have a n e g a t i v e e f f e c t on manganese a b s o r p t i o n . A n i m a l o r i g i n p r o d u c t s such as eggs, m i l k , f i s h , r e d meats and p o u l t r y c o n t a i n low amounts o f manganese. A b s o r p t i o n o f such m i n e r a l s as i r o n , copper, phosphorus and c a l c i u m i s s u p e r i o r from a n i m a l s p r o d u c t s t h a n from p l a n t - o r i g i n foods. As r e p o r t e d by K i e s e t a l . ( i n t h i s b o o k ) , manganese a p p a r e n t l y i s b e t t e r absorbed by humans from meals c o n t a i n i n g meat and f i s h t h a n from those c o n t a i n i n g p l a n t - p r o t e i n replacement p r o d u c t s . Because o f t h e low c o n t e n t


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Table I .

Comparative Manganese Contents o f Foods

Food Item


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M i l k and m i l k p r o d u c t s Cheese, American p r o c e s s e d Meat, p o u l t r y , f i s h , eggs B e e f , ground, cooked B e e f , chuck, o v e n - r o a s t e d Chicken, oven-roasted Frankfurters Fish f i l l e t Egg, s o f t b o i l e d Legumes and n u t s Pork and beans, canned Peanut b u t t e r G r a i n s and g r a i n p r o d u c t s R i c e , w h i t e , e n r i c h e d , cooked White b r e a d , e n r i c h e d Corn bread Biscuits Whole wheat bread Fruits Peaches, canned A p p l e s a u c e , canned F r u i t c o c k t a i l , canned P e a r s , canned C h e r r i e s , sweet Vegetables Coleslaw with dressing Cauliflower French f r i e s Mashed p o t a t o e s Boiled potatoes S p i n a c h , canned o r f r o z e n Mixed d i s h e s B e e f - v e g e t a b l e stew P i z z a , cheeze C h i l i con c a r n e C h i c k e n noodle c a s s e r o l e V e g e t a b l e beef soup Desserts Y e l l o w cake Pumpkin p i e Gelatin dessert

mg Mn/100 g F o o d

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0.0464 0.019 0.025 0.046 0.024 0.058 0.037 0.315 1.322 0.807 0.376 0.315 0.244 1.120 0.017 0.014 0.122 trace 0.085 0.093 0.102 0.150 0.075 0.083 0.501 0.101 0.259 0.140 0.140 0.181 0.390 0.620 0.005

^ h e s e v a l u e s were r e c a l c u l a t e d from t h o s e r e p o r t e d by Tack (50) and a r e i n r e a s o n a b l y good agreement w i t h t h o s e r e p o r t e d by P e n n i n g t o n e t a l . (32) and Gormican e t a l . ( 3 8 ) .


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MANGANESE

o f manganese i n meat and f i s h , t h i s i m p l i e s manganese a b s o r p t i o n and r e t e n t i o n from these p r o d u c t s i s e x c e l l e n t and i m p l i e s t h a t these a n i m a l o r i g i n p r o d u c t s enhance u t i l i z a t i o n o f manganese s u p p l i e d by p l a n t - o r i g i n p r o d u c t s as w e l l .


Methods o f E v a l u a t i o n o f Manganese S t a t u s Most s t u d i e s on f a c t o r s a f f e c t i n g manganese needs o f human s u b j e c t s have employed t h e manganese b a l a n c e t e c h n i q u e d u r i n g s h o r t - t e r m f e e d i n g p e r i o d s r a n g i n g from f i v e t o 14 days. However, measurements of o t h e r t i s s u e , b l o o d o r u r i n e components might be o f v a l u e i n assessment o f n u t r i t i o n a l s t a t u s o f humans o r a n i m a l s . F o r example, c h i l d r e n w i t h l e a r n i n g d i s a b i l i t i e s have been r e p o r t e d t o have h i g h h a i r manganese l e v e l s ( 3 9 ) , e l e v a t e d b l o o d serum l e v e l s o f manganese have been r e p o r t e d i n such d i s e a s e s t a t e s as c o n g e s t i v e h e a r t f a i l u r e ( 4 0 ) , i n f e c t i o n s (40) and A l z h e i m e r - l i k e d i s e a s e s (41) and e l e v a t e d manganese c o n c e n t r a t i o n s i n whold b l o o d have been found i n i n d i v i d u a l s w i t h e x c e s s manganese i n t a k e (42,43), rheumatoid a r t h r i t i s (44) and i r o n - d e f i c i e n c y anemia ( 4 5 ) . Whole b l o o d manganese l e v e l s o f many but n o t a l l a d u l t s w i t h c o n v u l s i v e d i s o r d e r s have been found t o be lower than i n normal c o n t r o l s ( 4 6 ) . B a s i s f o r Manganese "Safe I n t a k e L e v e l s " The Food and N u t r i t i o n B o a r d , N a t i o n a l Research C o u n c i l , N a t i o n a l Academy o f S c i e n c e s (47) has l i s t e d s a f e i n t a k e l e v e l s o f manganese a l t h o u g h i n f o r m a t i o n was, a t t h e time o f t h e 1980 l i s t i n g , t o o f r a g m e n t a r y f o r exact recommendations t o be made. These manganese " s a f e i n t a k e l e v e l " l i s t i n g s were as f o l l o w s : 2.5-5.0 mg/day f o r a d u l t s , 0.7-1.0 mg/day f o r i n f a n t s and 1.0-5.0 mg/day f o r t o d d l e r s . I n l a b o r a t o r y c o n t r o l l e d s t u d i e s , p o s i t i v e manganese b a l a n c e s ( c a l c u l a t e d from the f o r m u l a : manganese b a l a n c e = d i e t a r y manganese - f e c a l manganese - u r i n e manganese) have been observed when s u b j e c t s were m a i n t a i n e d a t 2.5 mg manganese/day o r h i g h e r but n e g a t i v e b a l ances o c c u r r e d when s u b j e c t s were f e d 0.7 mg manganese/day ( 4 8 ) . An e x t e n s i v e r e v i e w o f t h e l i t e r a t u r e r e l a t i v e t o human s t u d i e s on manganese r e q u i r e m e n t s o f humans i s p r e s e n t e d by F r e e l a n d - G r a v e s e t a l . i n t h i s volume. A f a c t o r i a l method f o r e s t i m a t i o n o f manganese r e q u i r e m e n t s o f humans i s g i v e n by these a u t h o r s . I n r e c e n t s t u d i e s r e p o r t e d by Rao and Rao ( 4 9 ) , I n d i a n men r e q u i r e d 3.72 mg manganese/day t o m a i n t a i n manganese b a l a n c e . In s t u d i e s conducted a t t h e U n i v e r s i t y o f N e b r a s k a , American a d u l t s u b j e c t s a l s o f a i l e d t o be i n manganese b a l a n c e when manganese i n t a k e was m a i n t a i n e d a t 2.5 mg/day ( 3 1 ) . C u r r e n t e s t i m a t i o n o f d i e t a r y manganese adequacy may be t o o low, p a r t i c u l a r l y i f d i e t s c o n t a i n s u b s t a n t i a l amounts o f f i b e r o r a r e based l a r g e l y on p l a n t p r o d u c t s . However, f o r meat c o n t a i n i n g d i e t s , t h e c u r r e n t e s t i m a t e d l e v e l s o f adequacy may be q u i t e adequate. Conclusion W h i l e manganese n u t r i t i o n a l s t a t u s i s n o t c u r r e n t l y r e c o g n i z e d as a problem i n t h e U n i t e d S t a t e s o r i n t h e r e s t o f t h e w o r l d , c e r t a i n groups may have l e s s than o p t i m a l manganese n u t r i t i o n a l s t a t u s


1.

KIES


7

because o f lower i n t a k e s than p r e v i o u s l y s u s p e c t e d from s e l f s e l e c t e d d i e t s . There i s a need f o r e s t a b l i s h m e n t o f manganese r e q u i r e m e n t s f o r a l l age/sex groups consuming d i e t based on c u r r e n t or recommended food p a t t e r n s . F u r t h e r m o r e , t h e f e a s a b i l i t y o f e x p r e s s i n g manganese c o n t e n t s o f foods on t h e b a s i s o f b i o l o g i c a l l y a v a i l a b l e manganese c o n t e n t r a t h e r than on c h e m i c a l l a b o r a t o r y v a l u e s deserves c o n s i d e r a t i o n . Acknowledgment s


P u b l i s h e d as U n i v e r s i t y o f Nebraska A g r i c u l t u r a l Research D i v i s i o n J o u r n a l A r t i c l e S e r i e s No. 8062a. Supported by Nebraska A g r i c u l t u r a l Research D i v i s i o n P r o j e c t 91-031 and USDA, CSRS R e g i o n a l Research P r o j e c t W-143.

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Nutritional Bioavailability of Manganese - ACS Publications

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